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Extracellular DNA secreted in yeast cultures is metabolism-specific and inhibits cell proliferation.

ABSTRACT: Extracellular DNA (exDNA) can be actively released by living cells and different putative functions have been attributed to it. Further, homologous exDNA has been reported to exert species-specific inhibitory effects on several organisms. Here, we demonstrate by different experimental evidence, including ¹H-NMR metabolomic fingerprint, that the growth rate decline in Saccharomyces cerevisiae fed-batch cultures is determined by the accumulation of exDNA in the medium. Sequencing of such secreted exDNA represents a portion of the entire genome, showing a great similarity with extrachromosomal circular DNA (eccDNA) already reported inside yeast cells. The recovered DNA molecules were mostly single strands and specifically associated to the yeast metabolism displayed during cell growth. Flow cytometric analysis showed that the observed growth inhibition by exDNA corresponded to an arrest in the S phase of the cell cycle. These unprecedented findings open a new scenario on the functional role of exDNA produced by living cells.

SUBMITTER: de Alteriis E

PROVIDER: S-EPMC10695634 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Extracellular DNA secreted in yeast cultures is metabolism-specific and inhibits cell proliferation.

de Alteriis Elisabetta E Incerti Guido G Cartenì Fabrizio F Chiusano Maria Luisa ML Colantuono Chiara C Palomba Emanuela E Termolino Pasquale P Monticolo Francesco F Esposito Alfonso A Bonanomi Giuliano G Capparelli Rosanna R Iannaccone Marco M Foscari Alessandro A Landi Carmine C Parascandola Palma P Sanchez Massimo M Tirelli Valentina V de Falco Bruna B Lanzotti Virginia V Mazzoleni Stefano S

Microbial cell (Graz, Austria) 20231123 12

Extracellular DNA (exDNA) can be actively released by living cells and different putative functions have been attributed to it. Further, homologous exDNA has been reported to exert species-specific inhibitory effects on several organisms. Here, we demonstrate by different experimental evidence, including <sup>1</sup>H-NMR metabolomic fingerprint, that the growth rate decline in <i>Saccharomyces cerevisiae</i> fed-batch cultures is determined by the accumulation of exDNA in the medium. Sequencing ...[more]

PMID: 38053574

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Project description:In vitro construction is a major trend involved in cartilage regeneration and repair. Satisfactory in vitro cartilage regeneration depends on a suitable culture system. Current chondrogenic culture systems with a high content of transforming growth factor beta-1 effectively promote cartilaginous extracellular matrix (ECM) production but inhibit chondrocyte survival. As is known, inhibition of the c-Jun N-terminal kinase (JNK) signaling pathway acts in blocking the progression of osteoarthritis by reducing chondrocyte apoptosis and cartilage destruction. However, whether inhibiting JNK signaling resists the inhibitory effect of current chondrogenic medium (CM) on cell survival and affects in vitro auricular cartilage regeneration (including cell proliferation, ECM synthesis, and degradation) has not been investigated. In order to address these issues and optimize the chondrogenic culture system, we generated a three-dimensional in vitro auricular cartilage regeneration model to investigate the effects of SP600125 (a JNK-specific inhibitor) on chondrocyte proliferation and ECM metabolism. SP600125 supplementation efficiently promoted cell proliferation at both cellular and tissue levels and canceled the negative effect of our chondrogenic culture system on cell survival. Moreover, it significantly inhibited ECM degradation by reducing the expressions of tumor necrosis factor-alpha, interleukin-1-beta, and matrix metalloproteinase 13. In addition, SP600125 inhibited ECM synthesis at both cellular and tissue levels, but this could be canceled and even reversed by adding chondrogenic factors; yet this enabled a sufficient number of chondrocytes to be retained at the same time. Thus, SP600125 had a positive effect on in vitro auricular cartilage regeneration in terms of cell proliferation and ECM degradation but a negative effect on ECM synthesis, which could be reversed by adding CM. Therefore, a combination of SP600125 and CM might help in optimizing current chondrogenic culture systems and achieve satisfactory in vitro cartilage regeneration by promoting cell proliferation, reducing ECM degradation, and enhancing ECM synthesis.

Dataset Information

Extracellular DNA secreted in yeast cultures is metabolism-specific and inhibits cell proliferation.

Publications

Extracellular DNA secreted in yeast cultures is metabolism-specific and inhibits cell proliferation.

Similar Datasets

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